Does the Genomic Landscape of Species Divergence in Phaseolus Beans Coerce Parallel Signatures of Adaptation and Domestication?

Exploring the genomic architecture of species and populations divergence aids understanding how lineages evolve and adapt, and ultimately can show the repeatability of evolutionary processes. Yet, the genomic signatures associated with divergence are still relatively unexplored, leading to a knowledge gap on whether species divergence ultimately differs in its genetic architecture from divergence at other spatial scales (i.e., populations, ecotypes). Our goal in this research was to determine whether genomic islands of speciation are more prone to harbor within-species differentiation due to genomic features, suppressed recombination, smaller effective population size or increased drift, across repeated hierarchically nested levels of divergence. We used two species of Phaseolus beans with strong genepool and population sub-structure produced by multiple independent domestications each especially in Andean and Mesoamerican / Middle American geographies. We genotyped 22,531 GBS-derived SNP markers in 209 individuals of wild and cultivated Phaseolus vulgaris and Phaseolus lunatus. We identified six regions for species-associated divergence. Out of these divergence peaks, 21% were recovered in the four within-species between-genepool comparisons and in the five within-genepool wild-cultivated comparisons (some of the latter did retrieve genuine signatures of the well described multiple domestication syndromes). However, genomic regions with overall high relative differentiation (measured by FST) coincided with regions of low SNP density and regions of elevated delta divergence between-genepools (ΔDiv), independent of the scale of divergence. The divergence in chromosome Pv10 further coincided with a between-species pericentric inversion. These convergences suggest that shared variants are being recurrently fixed at replicated regions of the genome, and in a similar manner across different hierarchically nested levels of divergence, likely as result of genomic features that make certain regions more prone to accumulate islands of speciation and within-species divergence. In summary, neighboring signatures of speciation, adaptation and domestication in Phaseolus beans are influenced by ubiquitous genomic constrains, which may continue to fortuitously shape genomic differentiation at various others scales of divergence.

Testing Domestication Scenarios of Lima Bean (Phaseolus lunatus L.) in Mesoamerica: Insights from Genome-Wide Genetic Markers.

Plant domestication can be seen as a long-term process that involves a complex interplay among demographic processes and evolutionary forces. Previous studies have suggested two domestication scenarios for Lima bean in Mesoamerica: two separate domestication events, one from gene pool MI in central-western Mexico and another one from gene pool MII in the area Guatemala-Costa Rica, or a single domestication from gene pool MI in central-western Mexico followed by post-domestication gene flow with wild populations. In this study we evaluated the genetic structure of the wild gene pool and tested these two competing domestication scenarios of Lima bean in Mesoamerica by applying an ABC approach to a set of genome-wide SNP markers. The results confirm the existence of three gene pools in wild Lima bean, two Mesoamerican gene pools (MI and MII) and the Andean gene pool (AI), and suggest the existence of another gene pool in central Colombia. The results indicate that although both domestication scenarios may be supported by genetic data, higher statistical support was given to the single domestication scenario in central-western Mexico followed by admixture with wild populations. Domestication would have involved strong founder effects reflected in loss of genetic diversity and increased LD levels in landraces. Genomic regions affected by selection were detected and these may harbor candidate genes related to domestication.

Domestication of small-seeded lima bean (Phaseolus lunatus L.) landraces in Mesoamerica: evidence from microsatellite markers.

Previous studies have suggested that the Mesoamerican small-seeded landraces of Lima bean may have been domesticated more than once in Mesoamerica, once in central-western Mexico and another one in an area between Guatemala and Costa Rica. However, these findings were based on sequencing of only one locus from nuclear DNA, and additional confirmation was needed. Here we contribute with additional data on the origin of the Mesoamerican landraces and document the founder effect due to domestication. We characterized 62 domesticated, 87 wild and six weedy Lima bean accessions with ten microsatellite loci. Genetic relationships were analyzed using genetic distances and Bayesian clustering approaches. Domestication bottlenecks were documented using inter-population comparisons and M ratios. The results support at least one domestication event in the area of distribution of gene pool MI in central-western Mexico and also show that some landraces are genetically related to wild accessions of gene pool MII. Also, our data support founder effects due to domestication in Mesoamerican Lima bean landraces. Although we could not establish more specifically the place of origin of the Mesoamerican Lima bean landraces, our results show that these are not a genetically homogeneous group, a finding that may be compatible with a scenario of more than one domestication event accompanied by gene flow. The complex genetic makeup of landraces that we found indicates that a more comprehensive geographic and genomic sampling is needed in order to establish how domestication processes and gene flow have shaped the current genetic structure of landraces.

Genetic structure within the Mesoamerican gene pool of wild Phaseolus lunatus (Fabaceae) from Mexico as revealed by microsatellite markers: Implications for conservation and the domestication of the species.

UNLABELLED: • PREMISE OF THE STUDY: Understanding genetic structure in wild relatives of a crop is important for crop improvement and conservation. Recently, two gene pools (MI and MII) were reported in wild Lima bean (Phaseolus lunatus) from Mexico, a domestication center of Mesoamerican landraces. However, the evidence was based on limited genomic sampling. Here we sought to confirm the existence of these two gene pools by increased genome and population sampling.• METHODS: We characterized 67 wild populations of P. lunatus from Mexico with 10 microsatellite loci and studied the genetic structure by means of AMOVA, cluster analyses, assignment tests, and a georeferenced map.• KEY RESULTS: AMOVA indicated that most of the variation is found among populations (77%) rather than within populations (23%). Assignment tests were key to confirm not only the presence of the two gene pools (MI and MII) in Mexico, but also to propose the possible existence of two subgroups within MI (MIa and MIb). While MI and MII are mainly divergent geographically, MIa and MIb overlap in their distribution. Admixed individuals, which may represent cases of gene flow among gene pools, were detected.• CONCLUSIONS: Our results show that the genetic structure of wild Lima bean in Mexico is more complex than previously thought and propose the presence of three gene pools (MIa, MIb, and MII), each one possessing relatively high levels of genetic diversity. We still need additional evidence, however, to confirm without doubt the split of the gene pool MI into subgroups MIa and MIb.